Inhibition of phagosome maturation by mycobacteria does not interfere with presentation of mycobacterial antigens by MHC molecules

Journal of Immunology

Volumn 179, Issue 3, 2007, Pages 1825-1833

  Majlessi, Laleh ^a,b   Combaluzier, Benoit ^c   Albrecht, Imke ^c   Garcia, Jessica E ^a,b   Nouze, Clémence ^a,b   Pieters, Jean ^c   Leclerc, Claude ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; ACYLTRANSFERASE; ANTIGEN 85A, MYCOBACTERIUM TUBERCULOSIS; BACTERIAL ANTIGEN; H2 ANTIGEN; HLA ANTIGEN CLASS 2; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL STRAIN; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME; MACROPHAGE; MOUSE; MYCOBACTERIUM BOVIS; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; ANIMAL; ANTIGEN PRESENTATION; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; DOWN REGULATION; ENZYMOLOGY; IMMUNOLOGY; INTRACELLULAR FLUID; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY;

ACYLTRANSFERASES; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, BACTERIAL; CELL DIFFERENTIATION; CELLS, CULTURED; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DENDRITIC CELLS; DOWN-REGULATION; FEMALE; H-2 ANTIGENS; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTRACELLULAR FLUID; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYCOBACTERIUM BOVIS; PHAGOSOMES; PROTEIN-SERINE-THREONINE KINASES; VIRULENCE FACTORS;

EID: 34548653644     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.3.1825     Document Type: Article

References (57)

1. Kaufmann, S. H. 2006. Tuberculosis: back on the immunologists' agenda. Immunity 24: 351-357.
2. Peters, P. J., J. J. Neefjes, V. Oorschot, H. L. Ploegh, and H. J. Geuze. 1991. Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature 349: 669-676.
3. Tulp, A., D. Verwoerd, B. Dobberstein, H. L. Ploegh, and J. Pieters. 1994. Isolation and characterization of the intracellular MHC class II compartment. Nature 369: 120-126.
4. Amigorena, S., J. R. Drake, P. Webster, and I. Mellman. 1994. Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature 369: 113-120.
5. Bryant, P. W., A. M. Lennon-Dumenil, E. Fiebiger, C. Lagaudriere-Gesbert, and H. L. Ploegh. 2002. Proteolysis and antigen presentation by MHC class II molecules. Adv. Immunol. 80: 71-114.
6. Ramachandra, L., R. S. Chu, D. Askew, E. H. Noss, D. H. Canaday, N. S. Potter, A. Johnsen, A. M. Krieg, J. G. Nedrud, W. H. Boom, and C. V. Harding. 1999. Phagocytic antigen processing and effects of microbial products on antigen processing and T-cell responses. Immunol. Rev. 168: 217-239.
7. Kovacsovics-Bankowski, M., and K. L. Rock. 1995. A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 267: 243-246.
8. Guermonprez, P., L. Saveanu, M. Kleijmeer, J. Davoust, P. Van Endert, and S. Amigorena. 2003. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 425: 397-402.
9. Gagnon, E., S. Duclos, C. Rondeau, E. Chevet, P. H. Cameron, O. Steele-Mortimer, J. Paiement, J. J. Bergeron, and M. Desjardins. 2002. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110: 119-131.
10. Roy, C. R., S. P. Salcedo, and J. P. Gorvel. 2006. Pathogen-endoplasmic- reticulum interactions: in through the out door. Nat. Rev. Immunol. 6: 136-147.
11. Armstrong, J. A., and P. D. Hart. 1971. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J. Exp. Med. 134: 713-740.
12. Clemens, D. L., and M. A. Horwitz. 1995. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J. Exp. Med. 181: 257-270.
13. Clemens, D. L., and M. A. Horwitz. 1996. The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J. Exp. Med. 184: 1349-1355.
14. Xu, S., A. Cooper, S. Sturgill-Koszycki, T. van Heyningen, D. Chatterjee, I. Orme, P. Allen, and D. G. Russell. 1994. Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J. Immunol. 153: 2568-2578.
15. Clemens, D. L., B. Y. Lee, and M. A. Horwitz. 2000. Mycobacterium tuberculosis and Legionella pneumophila phagosomes exhibit arrested maturation despite acquisition of Rab7. Infect. Immun. 68: 5154-5166.
16. Sturgill-Koszycki, S., P. H. Schlesinger, P. Chakraborty, P. L. Haddix, H. L. Collins, A. K. Fok, R. D. Allen, S. L. Gluck, J. Heuser, and D. G. Russell. 1994. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263: 678-681.
17. Ferrari, G., H. Langen, M. Naito, and J. Pieters. 1999. A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97: 435-447.
18. Ramachandra, L., E. Noss, W. H. Boom, and C. V. Harding. 2001. Processing of Mycobacterium tuberculosis antigen 85B involves intraphagosomal formation of peptide-major histocompatibility complex II complexes and is inhibited by live bacilli that decrease phagosome maturation. J. Exp. Med. 194: 1421-1432.
19. Barker, L. P., K. M. George, S. Falkow, and P. L. Small. 1997. Differential trafficking of live and dead Mycobacterium marinum organisms in macrophages. Infect. Immun. 65: 1497-1504.
20. Walburger, A., A. Koul, G. Ferrari, L. Nguyen, C. Prescianotto-Baschong, K. Huygen, B. Klebl, C. Thompson, G. Bacher, and J. Pieters. 2004. Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304: 1800-1804.
21. Nguyen, L., A. Walburger, E. Houben, A. Koul, S. Muller, M. Morbitzer, B. Klebl, G. Ferrari, and J. Pieters. 2005. Role of protein kinase G in growth and glutamine metabolism of Mycobacterium bovis BCG. J. Bacteriol. 187: 5852-5856.
22. Majlessi, L., M. Simsova, Z. Jarvis, P. Brodin, M. J. Rojas, C. Bauche, C. Nouze, D. Ladant, S. T. Cole, P. Sebo, and C. Leclerc. 2006. An increase in antimycobacterial Th1-cell responses by prime-boost protocols of immunization does not enhance protection against tuberculosis. Infect. Immun. 74: 2128-2137.
23. Albrecht, I., J. Gatfield, T. Mini, P. Jeno, and J. Pieters. 2006. Essential role for cholesterol in the delivery of exogenous antigens to the MHC class I-presentation pathway. Int. Immunol. 18: 755-765.
24. +-T-cell responses of Mycobacterium-infected mice to a newly identified major histocompatibility complex class I-restricted epitope shared by proteins of the ESAT-6 family. Infect. Immun. 71: 7173-7177.
25. + T cells specific for the TB10.4 protein correlates with protection against Mycobacterium tuberculosis infection. Infect. Immun. 74: 3396-3407.
26. Huygen, K., E. Lozes, B. Gilles, A. Drowart, K. Palfliet, F. Jurion, I. Roland, M. Art, M. Dufaux, J. Nyabenda, et al. 1994. Mapping of TH1 helper T-cell epitopes on major secreted mycobacterial antigen 85A in mice infected with live Mycobacterium bovis BCG. Infect. Immun. 62: 363-370.
27. + T-cell epitopic repertoire broader than that stimulated by Mycobacterium tuberculosis H37Rv infection. Infect. Immun. 66: 1527-1533.
28. + T-cell epitope specificity of the Th1 immune response to an antigen using a Salmonella enterica serovar typhimurium delivery vehicle. Infect. Immun. 68: 3079-3089.
29. Tulp, A., D. Verwoerd, and J. Pieters. 1993. Application of an improved density gradient electrophoresis apparatus to the separation of proteins, cells and subcellular organelles. Electrophoresis 14: 1295-1301.
30. Engering, A. J., M. Cella, D. Fluitsma, M. Brockhaus, E. C. Hoefsmit, A. Lanzavecchia, and J. Pieters. 1997. The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur. J. Immunol. 27: 2417-2425.
31. Cella, M., A. Engering, V. Pinet, J. Pieters, and A. Lanzavecchia. 1997. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 388: 782-787.
32. Wiker, H. G., and M. Harboe. 1992. The antigen 85 complex: a major secretion product of Mycobacterium tuberculosis. Microbiol. Rev. 56: 648-661.
33. Brodin, P., I. Rosenkrands, P. Andersen, S. T. Cole, and R. Brosch. 2004. ESAT-6 proteins: protective antigens and virulence factors? Trends Microbiol. 12: 500-508.
34. + T cells of mycobacteria growing in human macrophages. Science 260: 984-986.
35. Hmama, Z., R. Gabathuler, W. A. Jefferies, G. de Jong, and N. E. Reiner. 1998. Attenuation of HLA-DR expression by mononuclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterodimers. J. Immunol. 161: 4882-4893.
36. Noss, E. H., R. K. Pai, T. J. Sellati, J. D. Radolf, J. Belisle, D. T. Golenbock, W. H. Boom, and C. V. Harding. 2001. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J. Immunol. 167: 910-918.
37. Pieters, J. 1997. MHC class II compartments: specialized organelles of the endocytic pathway in antigen presenting cells. Biol. Chem. 378: 751-758.
38. Pieters, J. 1997. MHC class II restricted antigen presentation. Curr. Opin. Immunol. 9: 89-96.
39. Ferrari, G., A. M. Knight, C. Watts, and J. Pieters. 1997. Distinct intracellular compartments involved in invariant chain degradation and antigenic peptide loading of major histocompatibility complex (MHC) class II molecules. J. Cell Biol. 139: 1433-1446.
40. Tekaia, F., S. V. Gordon, T. Garnier, R. Brosch, B. G. Barrell, and S. T. Cole. 1999. Analysis of the proteome of Mycobacterium tuberculosis in silico. Tuber. Lung Dis. 79: 329-342.
41. Pym, A. S., P. Brodin, L. Majlessi, R. Brosch, C. Demangel, A. Williams, K. E. Griffiths, G. Marchal, C. Leclerc, and S. T. Cole. 2003. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat. Med. 9: 533-539.
42. Okkels, L. M., and P. Andersen. 2004. Protein-protein interactions of proteins from the ESAT-6 family of Mycobacterium tuberculosis. J. Bacteriol. 186: 2487-2491.
43. Trombetta, E. S., and I. Mellman. 2005. Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol. 23: 975-1028.
44. Davidson, H. W., and C. Watts. 1989. Epitope-directed processing of specific antigen by B lymphocytes. J. Cell Biol. 109: 85-92.
45. Watts, C., and H. W. Davidson. 1988. Endocytosis and recycling of specific antigen by human B cell lines. EMBO J. 7: 1937-1945.
46. Delamarre, L., M. Pack, H. Chang, I. Mellman, and E. S. Trombetta. 2005. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307: 1630-1634.
47. +-ATPases. J. Biol. Chem. 272: 29810-29820.
48. Pluger, E. B., M. Boes, C. Alfonso, C. J. Schroter, H. Kalbacher, H. L. Ploegh, and C. Driessen. 2002. Specific role for cathepsin S in the generation of antigenic peptides in vivo. Eur. J. Immunol. 32: 467-476.
49. Villadangos, J. A., R. J. Riese, C. Peters, H. A. Chapman, and H. L. Ploegh. 1997. Degradation of mouse invariant chain: roles of cathepsins S and D and the influence of major histocompatibility complex polymorphism. J. Exp. Med. 186: 549-560.
50. Shi, G. P., J. S. Munger, J. P. Meara, D. H. Rich, and H. A. Chapman. 1992. Molecular cloning and expression of human alveolar macrophage cathepsin S, an elastinolytic cysteine protease. J. Biol. Chem. 267: 7258-7262.
51. Driessen, C., R. A. Bryant, A. M. Lennon-Dumenil, J. A. Villadangos, P. W. Bryant, G. P. Shi, H. A. Chapman, and H. L. Ploegh. 1999. Cathepsin S controls the trafficking and maturation of MHC class II molecules in dendritic cells. J. Cell Biol. 147: 775-790.
52. Blander, J. M., and R. Medzhitov. 2006. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 440: 808-812.
53. Houde, M., S. Bertholet, E. Gagnon, S. Brunet, G. Goyette, A. Laplante, M. F. Princiotta, P. Thibault, D. Sacks, and M. Desjardins. 2003. Phagosomes are competent organelles for antigen cross-presentation. Nature 425: 402-406.
54. Ojcius, D. M., L. Gapin, and P. Kourilsky. 1993. Dissociation of the peptide/ MHC class I complex: pH dependence and effect of endogenous peptides on the activation energy. Biochem. Biophys. Res. Commun. 197: 1216-1222.
55. Lewinsohn, D. M., J. E. Grotzke, A. S. Heinzel, L. Zhu, P. J. Ovendale, M. Johnson, and M. R. Alderson. 2006. Secreted proteins from Mycobacterium tuberculosis gain access to the cytosolic MHC class-I antigen-processing pathway. J. Immunol. 177: 437-442.
56. Schaible, U. E., F. Winau, P. A. Sieling, K. Fischer, H. L. Collins, K. Hagens, R. L. Modlin, V. Brinkmann, and S. H. Kaufmann. 2003. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat. Med. 9: 1039-1046.
57. Winau, F., S. Weber, S. Sad, J. de Diego, S. L. Hoops, B. Breiden, K. Sandhoff, V. Brinkmann, S. H. Kaufmann, and U. E. Schaible. 2006. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity 24: 105-117.